Leeuwenhoek (1693) was the first author to report on the osteocyte lacuna. The first observation of osteocyte lacuna raised the significance of geometry to bone microstructure by noting the necessity of proper direction of specimen cut to observe the pseudo-ellipsoidal shape of the lacuna (Leeuwenhoek, 1693). In the osteocyte lacuna, the osteocyte processes extend through the surrounding extracellular matrix (ECM) within so-called canaliculi (Enlow, 1962). Modern observations show canalicular distribution at the perilacunar region (Martin et al., 1998). Several hypotheses have been so far formulated relative to a correlation between densities of osteocyte lacunae and distributions of properties of bone tissue related to strain, remodeling or metabolism (Skedros et al., 2005). The osteocyte lacunae have been hypothesized to act as stress concentrators through their ellipsoidal contour and as fracture initiators when a crack forms at the apex by deformation (Currey, 1962; Piekarski, 1970). Reilly (2000) and O'Brien et al. (2005a and 2005b) observed micro-damage around the osteocyte lacunae with micro-cracks accumulating at a rate that increased with the strain/stress level. Prendergast and Huiskes (1996) and Bonivtch et al. (2007) investigated the perilacunar strain levels with homogeneous material modeling of the ECM.
Because carbonated apatite crystals in osteons locally follow the orientation of the adjacent collagen (Ascenzi A. et al., 1966), and because the collagen-apatite orientation is one of the variables that determines the mode of fracture (Simkin and Robin, 1974), collagen orientation is an important datum to understand fracture initiation, propagation, and arrest in osteons and in particular in connection with osteocyte lacunae. The osteon model of the present invention includes the collagen orientation datum at the lacunar-ECM interface, a new step in the long history of osteon modeling (from Gebhardt, 1906 to Jasiuk and Ostoja-Starzewski, 2004; Ascenzi and Lomovstev, 2006). Each of extinction or brightness of lamellae outside the perilacunar region denotes a specific dominant orientation of collagen in cross-section under circularly polarized light (Ascenzi and Lomovstev, 2006). Indeed, the dominant collagen orientation of so-called extinct lamellae forms small angles with the original osteon axis, while the dominant collagen orientation in bright lamellae forms larger angles. The osteon model presented here incorporates the collagen orientation in the lamella within and beyond the perilacunar region.
The present invention is based on the following: (i) the collagen orientation patterns along the lateral regions of the osteocyte lacuna do not differ in relation to type (extinct or bright) of lamellae on the osteonal cross-section under circularly polarized light; (ii) the generally circumambiently perpendicular orientation of collagen at the perilacunar equatorial section of the lacuna of both lamellar types reinforces bone tissue to better resist stress generated under tensional loading; and (iii) the tilt of the lacuna, radial and circumferential, depends on the lamellar type—e.g., the osteocyte lacuna is more likely to be tilted with respect to the lacunar walls in extinct lamella than in the bright lamella. At the apices of such lacuna, collagen is more likely to follow the adjacent canalicular orientation in the bright lamella, in order for the parallel apatite to reinforce the tissue. This would delay fracture initiation and therefore optimize tissue function.